Reports our experience of REAHs.
\\n\\n
More than half of the publishers listed alongside IntechOpen (18 out of 30) are Social Science and Humanities publishers. IntechOpen is an exception to this as a leader in not only Open Access content but Open Access content across all scientific disciplines, including Physical Sciences, Engineering and Technology, Health Sciences, Life Science, and Social Sciences and Humanities.
\\n\\nOur breakdown of titles published demonstrates this with 47% PET, 31% HS, 18% LS, and 4% SSH books published.
\\n\\n“Even though ItechOpen has shown the potential of sci-tech books using an OA approach,” other publishers “have shown little interest in OA books.”
\\n\\nAdditionally, each book published by IntechOpen contains original content and research findings.
\\n\\nWe are honored to be among such prestigious publishers and we hope to continue to spearhead that growth in our quest to promote Open Access as a true pioneer in OA book publishing.
\\n\\n\\n\\n
\\n"}]',published:!0,mainMedia:null},components:[{type:"htmlEditorComponent",content:'
Simba Information has released its Open Access Book Publishing 2020 - 2024 report and has again identified IntechOpen as the world’s largest Open Access book publisher by title count.
\n\nSimba Information is a leading provider for market intelligence and forecasts in the media and publishing industry. The report, published every year, provides an overview and financial outlook for the global professional e-book publishing market.
\n\nIntechOpen, De Gruyter, and Frontiers are the largest OA book publishers by title count, with IntechOpen coming in at first place with 5,101 OA books published, a good 1,782 titles ahead of the nearest competitor.
\n\nSince the first Open Access Book Publishing report published in 2016, IntechOpen has held the top stop each year.
\n\n\n\nMore than half of the publishers listed alongside IntechOpen (18 out of 30) are Social Science and Humanities publishers. IntechOpen is an exception to this as a leader in not only Open Access content but Open Access content across all scientific disciplines, including Physical Sciences, Engineering and Technology, Health Sciences, Life Science, and Social Sciences and Humanities.
\n\nOur breakdown of titles published demonstrates this with 47% PET, 31% HS, 18% LS, and 4% SSH books published.
\n\n“Even though ItechOpen has shown the potential of sci-tech books using an OA approach,” other publishers “have shown little interest in OA books.”
\n\nAdditionally, each book published by IntechOpen contains original content and research findings.
\n\nWe are honored to be among such prestigious publishers and we hope to continue to spearhead that growth in our quest to promote Open Access as a true pioneer in OA book publishing.
\n\n\n\n
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\r\n\tThe use of dyes and pigments is narrowly associated with everyday life. Since ancient times, people have been using various types of dyes and pigments for both aesthetic and practical applications. Typically, the coloration of various materials e.g. textiles, clay, plastics, etc. has been their main purpose. Yet, the scope of contemporary dyes and pigments has become significantly broader and there is constant interest in new products fulfilling numerous requirements parallel to their ability to act as colorants. This trend has led to the development of functional dyes.
\r\n\r\n\tIn recent years, novel dyes and pigments with hi-tech applications have been developed and there is a continuous demand for new products with better properties and/or broader application scope. Of particular interest is the development of dyes and pigments with environment-responsive aptitudes i.e. products that can undergo some structural modification as a result of external stimuli e.g. light, heat, pressure, pH-changes, etc. These stimuli-responsive functional dyes have in turn found application in sensor technologies, optical data storage, molecular switches, etc. Acknowledging these facts, this book aims to cover current state-of-the-art research and development in the remarkably important area of environment-responsive (multi)functional dyes and pigments.
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He later on spent two years in Marseille, France (September 2010–January 2013) working as a postodoctoral researcher at the Institute of Molecular Sciences, CNRS/Aix-Marseille University, in the field of water oxidation catalysts in the research group of Dr. Thierry Tron before moving to to Uppsala, Sweden in 2014. There he joined the group of Dr. Henrik Ottosson (Uppsala University) and he worked as a postdoc researcher and later as a researcher (Forskare) focusing on excited state (anti)aromaticity and graphene photochemistry-related research. His current research interests revolve around physical organic and materials chemistry with an emphasis on the chemistry and photochemistry of graphene and novel covalent organic frameworks as well as polymer chemistry. He is the author and coauthor of 24 scientific research papers, two book chapters and he has more than 35 contributions in international conference proceedings. Furthermore, he is an active referee of scientific peer-reviewed papers of world-class chemistry journals and he has acted as a scientific expert evaluating international research-grant proposals. Currently he works as a Senior Research Scientist at TdB Labs AB (Sweden) and specializes in polysaccharide modifications and derivatization placing particular interest in fluorescent dye polysaccharide-functionalizations.",institutionString:"TdB Labs",position:null,outsideEditionCount:0,totalCites:0,totalAuthoredChapters:"2",totalChapterViews:"0",totalEditedBooks:"0",institution:null}],coeditorOne:null,coeditorTwo:null,coeditorThree:null,coeditorFour:null,coeditorFive:null,topics:[{id:"8",title:"Chemistry",slug:"chemistry"}],chapters:[{id:"74730",title:"Treatment of Textile Dyeing Waste Water Using TiO2/Zn Electrode by Spray Pyrolysis in Electrocoagulation Process",slug:"treatment-of-textile-dyeing-waste-water-using-tio2-zn-electrode-by-spray-pyrolysis-in-electrocoagula",totalDownloads:63,totalCrossrefCites:0,authors:[null]}],productType:{id:"1",title:"Edited Volume",chapterContentType:"chapter",authoredCaption:"Edited by"},personalPublishingAssistant:{id:"247865",firstName:"Jasna",lastName:"Bozic",middleName:null,title:"Ms.",imageUrl:"https://mts.intechopen.com/storage/users/247865/images/7225_n.jpg",email:"jasna.b@intechopen.com",biography:"As an Author Service Manager, my responsibilities include monitoring and facilitating all publishing activities for authors and editors. 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It is a relatively new diagnosis, only added to the World Health Organization classification of tumors in 2005 [1].
Wenig and Heffner were the first to describe it in 1995 in a series of 31 cases [2]. They described it as “a proliferation of glands lined by multi-layered ciliated respiratory epithelium, often with admixed mucocytes, arising in direct continuity with the surface epithelium, which invaginated downward into the submucosa.”
The lesion is usually diagnosed in middle-aged patients. Clinically it may manifest as a solitary lesion or in association with sinonasal polyposis. The former is far less common than the latter. The lesion takes its origin either in the olfactory cleft, the posterior septum, or the rhinopharynx [1, 2, 3, 4, 5] Because the incidence, clinical signs, imaging, modality of treatment, outcomes, and pathogenesis seem to be quiet different between these two clinical patterns, we call the first ones “REAHs” and the second ones “REAH-like.” This terminology is proposed by Jankowski [3, 5] and Hawley [4] as well.
The purpose of this paper is to remind the histopathological characteristics and differential diagnosis of REAHs/REAH-like lesions and to report two different cohorts of patients (one with REAHs and the other with REAH like lesions), treated in the ENT department of the CHU UCL Namur.
Grossly, REAH looks like a “polypoid fleshy to firm mass with areas of induration.” It is yellow or white [6]. It may have varying sizes (Figures 1–3).
Gross appearance of a REAH.
REAHs: The glandular proliferation arises in direct continuity with the surface epithelium with invagination downward into the submucosa. Clusters of seromucinous glands are seen.
REAHs: Occasionally the gland lumina are filled with mucinous or eosinophilic amorphous material. It often demonstrates periglandular stromal hyalinization, and there is often a mixed inflammatory infiltrate within the stroma.
The histologic picture is dominated by the presence of a glandular proliferation with a polypoid appearance. The proliferation starts from the surface epithelium and tends to be submucosal.
The glands are lined by ciliated respiratory epithelium originating from the surface respiratory epithelium. The glands are typically round to oval in shape and were small to medium in size with prominent dilation. Stromal tissue separates the glands. The epithelium may be cuboidal or flat, and mucinous gland metaplasia is often seen. Occasionally the gland lumina are filled with mucinous or eosinophilic amorphous material. It often demonstrates periglandular stromal hyalinization, and there is often a mixed inflammatory infiltrate within the stroma.
In the literature we can find another type of REAH called COREAH. It is characterized by a chondro-osseous differentiation. Flavin [7] and Roffman [8] were the two first authors to publish this entity, respectively, in 2005 and 2006. Since then 11 cases have been reported [9, 10]. It can occur in children or adults.
The histological features are almost exactly the same as REAH, but COREAH has islands of immature hyaline cartilage interspersed throughout the lesion (Figures 4 and 5).
COREAH: Nasal chondromesenchymal hamartoma. Multiple tumor fragments with a mucosal surface and nodules of cartilage (in red).
Seromucinous hamartoma: The mass is covered by respiratory epithelium and is comprised of lobular or haphazard proliferations of small to large glands and ducts which are lined by a single layer of cuboidal or flattened epithelial cells.
Immunohistochemistry has not been used to an extensive degree in the diagnosis of REAH, and it is not absolutely necessary to use it to make the definitive diagnosis of it.
However, Ozolek et al. did an immunohistochemical study in which they examined the profile of REAH [11]. REAHs are positive for CK7, negative for CK20 and CDX-2, and positive for MIB1 and Ki67. p63 staining was seen in the basal cells of REAH, which had a low proliferation index. The use of Mindbomb 1 (MIB-1) is useful in distinguishing REAH from other neoplasms, since neoplasms tend to have a high proliferation index.
REAHs: Immunohistochemistry: Positivity for CK7 and negativity for CK20.
The differential diagnostic of REAHs concerns the inflammatory polyps, Schneiderian papillomas, seromucinous hamartoma, and low-grade non-intestinal adenocarcinoma.
Inflammatory polyps are certainly the most common lesions that are confused with REAHs.
The most notable clinical differences between REAHs and inflammatory polyps are the location and their gross appearance.
Inflammatory polyps are typically the clinical manifestation of a sinonasal polyposis. Nasal polyps are rarely isolated. They are multiple and bilateral and usually extrude from the middle and superior meati. They are rarely attached to the posterior septum. REAHs originate specifically from the olfactory cleft.
Nasal polyps are usually edematous and not indurated. On microscopy, both lesions can show fibroblastic and vascular proliferation, stromal edema, a mixed inflammatory cell infiltrate, and seromucinous gland proliferation. However, inflammatory polyps do not have florid adenomatoid proliferation and stromal hyalinization which, when present, favor REAHs (Figures 6–9).
Macroscopic and endoscopic view of a nasal polyp.
Endoscopic view: right and left nasal cavity: presence of nasal polyps in the middle and superior meati.
Inflammatory polyp with edematous inflammatory stroma and single-layered glands.
Inflammatory polyp showing inflammatory stroma without hyalinization.
This is the second important differential diagnosis of REAHs.
Schneiderian papillomas are benign epithelial neoplasms of the sinonasal tract. Their annual incidence ranges between 0.2 and 1.5/100,000 people per year.
They are classified in three types: exophytic/fungiform papilloma, endophytic/inverted papilloma, and oncocytic/cylindrical cell papilloma. The inverted type is the most common, accounting for nearly two thirds of the cases. We limit the description to this type.
It is mostly unilateral. It occurs mainly in adults during the fifth or sixth decade. There is a predilection for men.
Unlike inflammatory polyps and REAHs, inverted papillomas are considered true neoplasms. While REAHs tend to be located medial to the turbinate lamella, inverted papillomas have a predilection for the lateral wall of the nasal cavity or the paranasal cavities. Maxillary and ethmoid sinuses are the most common origins followed by the sphenoid and frontal sinuses. Even if inverted papillomas are benign histologic lesions, clinically they may be aggressive with a relatively strong potential for local destruction, high rate of recurrence (more or less 50%), and a risk of carcinomatous evolution. This transformation in squamous cell carcinoma can be synchrone or metachrone and more likely in case of recurrence. This malignant transformation has never been observed in the case of REAHs.
Human papilloma virus seems to be implicated in the pathogenesis of inverted papillomas. Chronic inflammation seems to be a favorizing factor in REAHs.
The treatment of inverted papilloma requires a more extensive and radical excision with a subperiosteal dissection and a drilling of the base of implantation. Endonasal medial maxillectomy is the golden standard for maxillary sinus origin. Recurrence is more likely in frontal sinus papillomatosis due to the localization and the difficulty to completely eradicate the lesion. The surgical treatment for REAHs is a complete excision without ethmoidectomy.
Grossly, inverted papilloma looks like a reddish-gray lobulated tumor, more firm than an inflammatory polyp, with a fairly characteristic “raspberry” aspect (Figure 10).
Endoscopic view of an inverted papilloma originating from the left maxillary sinus.
Histologically inverted papillomas have an endophytic growth pattern. There is an invagination of stratified squamous epithelium with an admixture of mucin containing cells and microcysts. The epithelium may be of squamous, transitional, or respiratory type. The endophytic growth of squamous epithelium is not seen in REAH. Transmigrating neutrophils and neutrophilic microabscesses may be seen. Occasional mitoses may be seen in the basal layer. Mild to moderate atypia may be seen. Edema or chronic inflammatory infiltrate is present in the stroma (Figures 11–13).
Low magnification: typical view of an IP: it shows an endophytic growth pattern consisting of markedly thickened squamous epithelial proliferation growing downward into the underlying connective tissue stroma to form large clefts, ribbons, and islands. Note the absence of mucoserous glands. Delicate basement membrane.
Immunohistochemistry: high power shows the epithelium to be composed of pseudostratified columnar cells/positivity of MIB1 in the basal cells.
Immunohistochemistry: high power/positivity of CK7.
Seromucinous hamartoma is another subtype of hamartoma, recently described. It is a benign lesion of the sinonasal tract as well, located in the posterior nasal cavity or rhinopharynx frequently associated to REAHs. Since its description in 1974 [12], only a small number of additional cases have been reported.
The lesion occurs equally in men and women. Patients are middle-aged to elderly (mean age 50–60) and have complaints with nasal obstruction or nosebleeds. Surgical excision is the treatment of choice. It is included in the differential diagnosis of low grade epithelial proliferations of the sinonasal tract. The differentiation with low-grade non-intestinal adenocarcinoma can be tricky.
Histologically, the mass looks like a benign lesion. Lobular or haphazard proliferations of small to large glands and ducts lined by a single layer of cuboidal or flattened epithelial cells are visualized. Eosinophilic secretions are often present within tubules. The surrounding stroma often contains a lymphoplasmocytic inflammatory infiltrate. Periglandular hyalinization can be observed. There are no features suggesting a malignancy. There are no nuclear atypia.
Seromucinous hamartomas are positive for CK7 and CK19 and negative for CK14 and CK20. The serous glands are usually S100 positive and negative for p63 and muscle-specific antigen.
Sinonasal adenocarcinoma is the third differential diagnosis for REAH. It accounts for approximately 20% of all sinonasal malignancies and is classified into intestinal and non-intestinal salivary and non-salivary types. Intestinal adenocarcinomas (also called ITAC) take their origin in the olfactory cleftl and then extend into the ethmoid sinus, the orbit, or the anterior cranial fossa. It is an occupational disease; they typically occur in woodworkers. They look like an irregular exophytic pink necrotic and friable mass bulging into the nasal cavity located between the nasal septum and the turbinate lamella.
On microscopy, papillary and colonic types are the most common architectures. Differentiating ITAC from REAH is usually not difficult as the cell types, high-grade features, and increased mitotic index are characteristics for ITAC. ITAC is positive for CK20 and MIB1 and negative for CK7 (Figure 14).
Intestinal-type adenocarcinoma: Immunohistochemistry—Positivity for CK20, CK7, and MIB1.
On the other hand, low-grade non-intestinal adenocarcinomas (LGSNAC) are less common and less invasive. There is no sex or racial predilection. There is no association with wood dust exposure. They have no tendency to give systemic metastasis. However, they have a potential for local invasion and destruction of tissue. Extensive surgery is recommended to be associated with radiotherapy in some cases.
Histologically, the mass originates from the surface epithelium and the seromucinous glands of the submucosa. It consists of glandular proliferations lined by cuboidal to columnar cells which are usually monomorphic and cytologically bland. It forms a diverse group of bland tubular and/or papillary tumors. Mitoses are rare. Necrosis, perineural invasion, and lymphovascular invasion are absent. The stroma contains an inflammatory infiltrate as in REAHs.
Immunohistochemistry shows the positivity for CK7 and S100 and negativity for CK20 and CDX2.
The main differential diagnosis is between LGSNAC and seromucinous hamartoma (Figure 15).
LGSNAC: Glandular proliferations lined by cuboidal to columnar cells which are usually monomorphic and cytologically bland.
This clinical presentation of REAHs is actually the less frequent.
Table 1 reports a cohort of eight cases diagnosed and treated in the ENT department of the CHU UCL Namur since 2008.
Patient | Gender | Side | Symptoms |
---|---|---|---|
Br, L. | Female | R/olfactory cleft | Asymptomatic dacryoscan; 2009 |
Sch, M. | Female | L/septal implantation | Unilateral nasal obstruction 2008 |
Van rent. M. | Female | X2/olfactory cleft | Bilateral nasal obstruction 2012 |
W. Jes. | Female Seromucinous hamartoma | R/sphenochoanal recess | Unilateral nasal obstruction 2012 |
B. Pat. | Female/COREAH | L/sphenochoanal recess | Unilateral nasal obstruction/nasal collapse 2019 |
H. C. | Female | L/olfactory cleft | Unilateral nasal obstruction 2019 |
Tr. M. | Female | R/olfactory cleft | Asymptomatic Ct finding 2019 |
N, A. | Male | X2 R > L | Allergic rhinitis; paucisymptomatic/nasal endoscopy/CT scan 2019 |
Reports our experience of REAHs.
There were seven women. The mean age was 65 years old. Ranges are 27 and 81.
There was one man: age 53 years old.
The lesions were unilateral in six patients (three left sided; three right sided) and bilateral in two.
Two patients were asymptomatic. REAH was diagnosed by nasal endoscopy and a sinus CT scanner performed for an assessment of epiphora, a case of nasal dysfunction and another one to rule out sinus disease associated to his allergic rhinitis.
The other patients complained with nasal obstruction and rhinorrhea.
REAHS originated from the olfactory cleft in six patients and from the anterior wall of the sphenoid sinus in two cases.
On nasal endoscopy the lesion looked fleshy, with no vascular component and no necrosis.
On imaging the lesion was solitary in the olfactory cleft. No chronic rhinosinusitis was present (Figure 16).
Comparison between CT scan and nasal endoscopy.
The MRI performed in three cases was not so helpful. There were no pathognomonic features whatever was the localization. In the literature, REAHs appear as a homogeneous mass with post-contrast enhancement on T1-weighted sequences as well as hyperintensity on T2-weighted images (Figure 17) [13].
MRI of a patient with bilateral REAHs: T1- and T2-weighted sequences.
The diagnosis of REAH was confirmed in all the cases by the pathologist.
In one case it was a COREAH, and in another case it was a seromucinous hamartoma. These two hamartomas were located in the posterior nasal fossa.
A biopsy was performed under local anesthesia in asymptomatic cases to make a formal diagnosis. For the other the diagnosis was made on the surgical specimen.
There was no clear etiologic factor that could have played a role in the development of REAH except in one patient suffering from allergic rhinitis. There was no concomitant chronic sinusitis, asthma, or aspirin intolerance.
Concerning the management, in two patients a wait and see attitude was proposed as the patient was not symptomatic. For the others an endoscopic resection of the lesion was performed under general anesthesia. The dissection was done in a subperiosteal plane. We have never drilled out the site of implantation. There was no need to do a full house ethmoidectomy.
Until now we have had no recurrence (Figure 18).
Illustration of a case with bilateral REAHs: pre- and postop imaging.
This is the second clinical pattern of REAHs, and certainly this is the most common type.
Table 2 reports a cohort of 16 patients diagnosed with such a pattern during the past 18 months.
Patient | Sex | Disease/surgery |
---|---|---|
S. Jac. | M | Asthma/rev surgery: REAH-like X2/draf III |
Fris. JL | M | Polypose XZ/revision ethmoidectomy/REAH: chronic otitis media |
Ros. G | M | Recurrent NP/asthma: REAHs/rev ethmoidectomy |
Hub. S. | M | Sever NP/complete ethmoidectomy |
L.; Th. | M | Asthma: seromucous otitis media/revision surgery/REAH |
Br. Cl. | M | Aspirin intolerance; asthma/recurrence |
De Ras.Ge. | M | Nasal polyposis and asthma /previous surgery |
Bran. Ar | M | Revison surgery for massive polyposis |
De pl. Ph | M | Nasal polyposis operated 3 times/no asthma |
Hou. Adr. | M | Recurrentpolyposis/rev ethmoidectomy |
Aig; Ph. | M | Recurrentpolyposis/allergic rhinitis/aspirin intolerance/:metabisulfite intolerance |
Mas. Cl | F | Revision surgery/asthma/aspirin intolerance |
Corl. W. | M | Primary severe nasal polyposis: no asthma: operated in 2013/REAHs |
Tri. Fr. | M | Ethmoidectomy 10 y ago/nasal polyposis/ REAHs |
V. Mo | F | Nasal polyposis /asthma/previous FESS/REAHs X2 |
Cohort of patients with REAH-like lesions.
The series includes 13 men and 2 women. The mean average is about 63 years old.
The majority of the patients are in the fifth and sixth decades.
All the patients suffer from a nasal polyposis. In two cases it was a massive primary polyposis. The other patients have a nasal polyposis operated in the past. The REAHs were diagnosed at the revision surgery.
Eight patients have concomitant asthma. Two patients have aspirin intolerance.
Two patients have allergic rhinitis.
Chronic inflammation plays a role in the development of REAHs in this clinical pattern.
REAHs are located in the olfactory cleft. Their macroscopic aspect is different than usual nasal polyps extruding from the ethmoid sinus. They are more fleshy and firm. There is no necrosis.
As the following pictures show, it is extremely difficult to differentiate with the fibroscopy REAHs and inflammatory polyps in case of recurrent nasal polyposis. The histologic examination of the surgical specimens is mandatory for this differentiation (Figure 19).
Comparison of the nasal endoscopy and the histological pattern. The inflammation in the stroma is much more important than in pure REAHs.
CT imaging findings are described in only a limited number of studies [1, 4, 5, 14]. Lima et al. [5], Hawley et al. [4], and Lee et al. (51 cases) [14] conclude that REAHs cause widening of the olfactory cleft more than 10 mm but generally do not cause bone erosion.
All the paranasal sinus cavities can be opaque as illustrated by the following pictures (Figures 20–22):
CT showing a severe nasal polyposis; widening of the olfactory cleft raises suspicion of REAHs.
Patient with REAHs in the olfactory cleft. She had a standard ethmoidectomy for nasal polyposis. We observe REAHs in the olfactory cleft. Correlation between CT scan and nasal endoscopy.
Typical CT scan showing the opacity of both olfactory clefts caused by REAHs.
Some patients have a long-standing disease; REAHs develop after the surgery with time. Some of them are attached to the anterior and superior portion of the nasal septum and cause blockage of the frontal sinus pathway or even thinning and erosion of the nasal bones.
Figure 23 show such an exceptional evolution.
Same patient with thinning and erosion of the nasal bones (arrows) and opacity of both frontal sinuses.
MRI can be of some help to rule out other lesions such as encephalocele, olfactory neuroblastoma, or glioma.
The management of REAHs associated with nasal polyposis must be discussed case by case.
A complete sphenoethmoidectomy is usually necessary to manage the recurrent nasal polyposis.
For the REAHs, debulking or better exenteration of the olfactory cleft must be considered. But we know that it can be tricky and risky for the skull base with a risk of CSF leak if the surgery is too aggressive. Resection of the REAHs is usually more bloody than during a polypectomy.
In the case of frontal opacity caused by REAHs attached to the anterior and superior septa, a Draf III procedure must be considered.
After surgery medical treatment of the nasal polyposis and asthma remains absolutely necessary to prevent or delay as much as possible recurrences.
REAHs and REAH-like lesions are relatively new clinical entities. Despite numerous publications they are still underdiagnosed. These lesions are located in the olfactory clefts. They can be isolated or in association with nasal polyposis typically in the case of recurrence after FESS.
The clinicians and pathologists must know these lesions. They are usually benign, but in some cases they are associated to frontal sinus blockage and widening of the nasal vault; loss of smell is common. The differential diagnosis includes diseases with more severe morbidities such as inverted papilloma, seromucinous hamartomas, and low-grade non-intestinal adenocarcinoma.
Histological examination of all the surgical specimens is necessary.
The treatment is dictated by the disease.
The extent of the surgery depends on the type and size of the REAHs and the associated disease.
It consists of a limited polypectomy or a complete exenteration of the olfactory cleft associated or not to a full house ethmoidectomy and even a Draf III procedure.
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Due to the advantages that microalgae offer over many other species, researchers and entrepreneurs have shown great interest in the development of production processes for biofuels, functional foods and bio-products from different species. Compared to terrestrial crops, these microorganisms have photosynthetic efficiency, growth rate and higher biomass production, consequently mass cultivation for commercial microalgae production can be carried out efficiently [5]. In addition, the cultivation of microalgae does not require arable soil, and can be grown in saline, brackish and wastewater and in harsh conditions, not competing with the production of food that is currently a major challenge for the production of first and second biofuels generation [6]. Therefore, competition for arable land with other crops, especially for human consumption, is greatly reduced.
Although most microalgae grow exclusively through photosynthesis, some species are mixotrophic and use extracellular organic carbon when a light source is not available [7]. Microalgae can be a source of several important compounds, including hydrogen and hydrocarbons, pigments and dyes, food and feed, biopolymers, biofertilizers, insecticides, neutraceuticals (foods capable of providing health benefits) and pharmacological compounds, in addition to being a potential biomass for production of biofuels [8].
Although the production of microalgae does not directly compete with food production and can be grown in harsh conditions, economic viability does not yet exist in many of the processes of industrial interest. However, the improvement and mastery of technologies capable of making inserted industrial processes viable become essential. Despite of the microalgae have a wide potential for production and applications, there are many obstacles to the biodiversity of these algae, such as mastery of technologies for production, genetic improvement research of strains more resistant to pathogens and economic viability in large-scale production [9, 10]. According to Georgianna and Mayfield [11], although promising, the success of inserting microalgae in the production of various products depends mainly on two important factors: high productivity and quality of biomass, as well as cost-effective production.
One of the viable solutions to reduce the costs of microalgae biomass production is to explore different forms of energy metabolism, highlighting the photoautotrophic, heterotrophic and mixotrophic for commercial production. Understanding these forms of metabolism allows the application of efficient crop strategies aimed at increasing the production of biomass and bioproducts on a large scale with cost optimization to couple the agroindustry waste treatment [7]. Microalgae are able to eliminate a variety of pollutants in wastewater mainly nitrogenated, phosphates and organic carbons [12].
Mixotrophic cultivation is a preferable microalgae growth mode for biomass production [13]. Compared to photoautotrophic and heterotrophic metabolism, mixotrophic cultures have been demonstrated many advantages, such as less risk of contamination, reduced cost and high biomass productivity. Even susceptible to contaminations, the use of photobioreactors minimizes this risk, but increases the cost of the process, which can be offset by the high biomass yield that can reach 5–15 g/L, being 3–30 times higher than those produced under autotrophic growth conditions [14, 15].
The use of waste for microalgae mixotrophic growth has been researched, mainly with the objective of expanding and diversifying in an alternative way the control and combating the inappropriate disposal of these in the respective industries, combined with the perspective of minimizing the operational costs of producing microalgae in large scale that are still considered high. The waste generated by the agribusiness has a high load of organic matter with high concentrations of Biochemical Oxygen Demand (BOD), Chemical Oxygen Demand (COD), ammonia, phosphates, suspended solids harmful to the environment, in addition to dissolved components such as sugars, fat and proteins originating from food, contributing to environmental pollution [16].
According to Patel et al. [7], research involving the mixotrophic cultivation of microalgae using organic matter as a source of carbon points to the production of high yields of biomass and biocomposites of industrial interest when compared to systems involving photoautotrophic and heterotrophic metabolisms. In this sense, recent studies have been carried out using agroindustrial waste to grow microalgae in a mixotrophic regime in order to minimize the cost of the biomass production process and treat the effluent adding value to the process, suggesting a microalgae biorefinery system [17].
Patel et al. [18] cultivated C. protothecoides UTEX-256 under mixotrophic conditions using dairy waste as source of carbon. The high CO2-emitting dairy industry obligated to treat waste and improve its carbon-footprints. In general, biochemical treatment was effective to remove respectively 99.7 and 91–100% of organic and inorganic pollutants and produce biomass and lipids fractions.
Xio-Bo Tan et al. [19] demonstrated that Chlorella pyrenoidosa (FACHB-9) cultivated under mixotrophic conditions using anaerobic digestate of sludge with an optimal addition of acidified starch wastewater improved biomass and lipids production by 0.5-fold (to 2.59 g·L−1) and 3.2-fold (87.3 mg·L−1 ·d−1), respectively. In addition, 62% of total organic carbon, 99% of ammonium and 95% of orthophosphate in mixed wastewater were effectively removed by microalgae.
Wang et al. [20] utilized glucose recovered from enzymatic hydrolysis of food waste as culture medium in mixotrophic cultivation of Chlorella sp. to obtain high levels of lipid and lutein. The algal biomass was 6.9 g L−1 with 1.8 g L−1 lipid and 63.0 mg L−1 lutein using hydrolysate with an initial glucose concentration of 20 g L − 1. Furthermore, lipid derived from microalgae biomass using food hydrolysate was at high quality in terms of biodiesel properties.
Due to the success of mixotrophic microalgae growth, the use of agro-industrial by-products stands out, adding value to production processes and reducing costs. The nutritional characteristics, availability and low cost of obtaining evidence the possibility of using the by-products in the cultivation of microalgae. This work reviews the mixotrophic cultivation system of microalgae using waste from agribusiness as a source of organic carbon, pointing out the benefits of this strategy as a solution to the environmental problems caused by these effluents, adding value to an industrial process for the production of biomass and biocompounds as biorefinery.
Microalgae is a generic term used to refer a widely diverse group of photosynthetic microorganisms [21]. There are several species of microalgae, which are found in aquatic environments of fresh water, brackish and saline [22]. Microalgae in general, have varying microscopic sizes, perform photosynthesis, use carbon dioxide as a nutrient source for growth, in addition to playing a fundamental role in ecosystems [23, 24, 25]. It is estimated that there are about 800 thousand species of microalgae, of which about 40 to 50 thousand are of scientific knowledge, which makes it an almost unexplored resource, demonstrating the great biodiversity of these algae [26, 27]. In addition, most species are not yet known and very few are used for any purpose.
The basic composition of microalgae is based on carbohydrates, lipids, proteins, ash and nucleic acids, in addition to chlorophyll and other protective pigments and light capture that provide high photosynthetic capacity, allowing conversion of up to 10% of energy in biomass [28]. In conventional plants, this percentage is higher when compared to other conventional plants, whose conversion is limited to a maximum of 5% [29]. The predominant elements in the biomass of microalgae are carbon, nitrogen and phosphorus and some metals such as iron, cobalt, zinc is also found [28].
In recent years, several researches have been carried out seeking to develop technologies for the elaboration and diversification of products based on microalgae. The growing expansion of these products is part of a wide range of utilities inserted in the most different commercial niches, expanding the possibilities of use and adding value to the market. According to Hu et al. [30], the global algae market is expected to be worth of about $ 1.1 billion by 2024.
Microalgae are inserted in a wide variety of species, distinguishing one from the other due to their biological structure. In this sense, these microorganisms offer potential possibilities for CO2 biofixation, remediation, effluent treatment, production of biofuels, high-value products including pharmaceuticals, food and neutraceutics [31].
According to Rizwan et al. [32], microalgae can be a source of antioxidant compounds, carotenoids, enzyme polymer, lipid, natural dye, polyunsaturated fatty acid, peptide, toxin and sterols, which are widely used in industry. In addition, they are used for the synthesis of antiviral, antimicrobial, antiviral, antibacterial and anticancer drugs [33].
Commercial microalgae cultivation systems are operated to produce mainly pigments and metabolites for nutritional supplements [34]. The algae that have technical and economic viability of production are Spirulina (Arthrospira) for supplements with a high protein content, Haematococcus as a source of astaxanthin and Dunaliella salina for the production of pro-vitamin A [31]. Spirulina represents 60% of all biomass produced on a large scale [35]. This species can be easily grown in tropical regions and is well adapted to extreme environments, being relatively less susceptible to contamination than other microalgae, making it the most favorable choice for large-scale production [36].
Spirulina consists mainly of proteins (50–70%), being widely used in human nutrition to combat malnutrition [37]. This species is rich in essential amino acids, beta-carotene, minerals, essential fatty acids, vitamins, polysaccharides, among others. Chlorella accumulate high concentrations of carotenoids (astaxanthin, lutein, β-carotene, violaxanthin and zeaxanthin), antioxidants, vitamins, polysaccharides, proteins, peptides and fatty acids [5, 38]. In addition to all the benefits mentioned, the bioactive compounds of microalgae can have a biological, immune, antiviral and anti-cancer properties, being highly active [39].
Global warming has been worrying environmentalists across the planet. Although there are different ways of capturing CO2, the biological method stands out as a potentially attractive alternative. The requirements for producing and obtaining biomass from microalgae are basically CO2 and a source of light, be it natural or artificial [2]. Carbon dioxide can be converted into organic matter by performing photosynthesis using sunlight as an energy source [40, 41, 42]. Microalgae are more efficient for fixing CO2 and have a higher productivity rate (ton/ha/year) when compared to terrestrial plants. In addition, CO2 biofixation can be combined with other processes, such as the treatment of organic waste, being advantageous in terms of economic viability and environmental sustainability. Microalgae can also be grown in nutrient-rich organic effluents, salt and brackish water, reducing the use of fertile land and fresh drinking water [43].
Studies involving the mixotrophic cultivation of microalgae using industrial residues from agro-industry as a source of organic carbon have been carried out to minimize the cost of biomass production, treat the effluent and promote CO2 biofixation [7]. In this sense, expanding the ways in which these residues are used, avoiding their incorrect disposal, minimizes the effects of environmental pollution and adds value to industrial processes, encouraging a cleaner and more sustainable bioeconomy.
Currently, fossil fuels represent the main source of energy in the world, but unsustainable and directly related to the pollution of air, land, water and climate change. The burning of fossil fuels consolidated to increase the atmospheric concentration of CO2 being directly associated with global warming. Allied to this, the future oil scarcity is a major challenge for scientists, motivating a constant search for technologies capable of producing clean and sustainable fuels [44]. Among many biomasses, microalgae represent a promising source for the production of clean renewable energy, as they are capable of fixing CO2 by performing photosynthesis with efficiency and productivity superior to that of conventional oilseeds and terrestrial plants used in the production of biodiesel and bioethanol. Among the available biomass sources, microalgae have been evaluated and investigated as generation third biomass, being researched to produce different types of biofuels, among which are biodiesel, bioethanol, bio-oil, char, hydrogen and synthesis gas [45]. Recent research involving the production of biofuels has been focused on third generation biomass, since the first and second raw materials are based on terrestrial cultures that compete with food production and can lead to food crises [46]. Algae biofuels are not yet obtained on a large scale due to the high cost of the process justifying the development of new technologies that can bring economic viability [47].
Bioremediation and biofuel production from waste resources by microalgae platform is mainly important to utilize abundantly available solar energy biofixing CO2 and treat effluents through the mixotrophic growth of microalgae [7]. Algal bioremediation is a good strategy to produce biomass for biofuels production while remediating wastes, also improving carbon-footprint through carbon capturing and utilization technology.
A microalgae biorefinery enables to integrate fractionation and conversion processes to transform biomass into bioproducts such as food, feed, chemicals, and bio-energy as optimization of the use of the microalgae for reducing waste production, and maximizes process profit. After lipid transesterification for biodiesel, the residual biomass can be used to produce other biofuels such as methane, bio-oil and ethanol or biocompounds for food and pharmaceutical industry [48].
There are currently four cultivation technologies in use for the production of commercial microalgae including open ponds and raceway ponds (open systems), photobioreactors and fermenters [49]. In open systems, microalgae are grown in open areas, including tanks, lakes, and ponds, deep channels, among others. In closed systems, crops are grown in transparent bioreactors, exposed to sunlight or artificial radiation for photosynthesis and fermenters.
Natural and artificial lakes and ponds, where most of the systems commonly used are large, shallow ponds and tanks, represent open pond systems. The main advantages of these systems are the ease of construction and operation when compared to photobioreactors and the possibility of operating hybrid processes involving the cultivation of algae associated with the treatment of wastewater. However, the disadvantages are inefficient light distribution, losses through evaporation, diffusion of CO2 into the atmosphere, contamination and the requirement for large areas of land [50]. Open ponds are currently in use for wastewater treatment and production of Dunaliella salina, characterized as a hybrid process. These systems are used by Ognis Australia Pty Ltd. to produce β-carotene from Dunaliella salina in Hutt Lagoon and Whyalla. In terms of surface area used, these are among the largest algae production systems in the world.
Closed or artificial ponds (circular ponds and raceway ponds) are more efficient than open systems for producing microalgae, since control over the production environment is much better than open ponds or extensive ponds. The cost of raceway ponds is higher than that of open lagoon systems, but lower than that of photobioreactors. These systems are the most used due to their potential to produce large quantities of biomass for commercial application. Raceway pond ponds are commonly used to grow Chlorella sp., Spirulina platensis, Haematococcus sp. and Dunaliella salina, with a biomass production rate of 60–100 mg of dry biomass/L/day [50]. Raceway ponds are used to produce Spirulina at Earthrise Nutraceuticals in the USA and Cyanotech Corp. in Hawaii [49].
Photobioreactors were designed to overcome the problems associated with open growth systems. It has been shown that cultivation of microalgae in these systems are capable of producing large amounts of biomass as they allow an effective control of process parameters, such as pH, temperature, CO2 concentration, level of contamination, among others. However, photobioreactors are much more expensive than open ponds and raceway ponds. Commercial photobioreactor productions include the production of H. pluvialis in Israel and Hawaii and C. vulgaris in Germany. Production costs are very high, reaching $ 100/kg [49]. As a result, biofuel production based entirely on photobioreactors is generally considered unlikely to be commercially viable [6, 49, 50].
Closed fermenters are used for the production of heterotrophic algae, where sugars or other simple carbon sources are used for growth instead of CO2 and light. Open fermenters similar to the fermenters used in the production of ethanol in industries are not suitable for the growth of algae, since these microorganisms have slow growth when compared to yeasts and bacteria. In the USA, India and China ω-3 fatty acids are produced from Thraustochytrids by heterotrophic fermentation through sugars and O2. As it is a high value-added product, it is sold for 100 $ /kg, which justifies the high cost of the process [49].
Microalgae have different growth metabolisms, which characterizes their versatility. Cultivation conditions define the metabolic route for the production of biocompounds, including proteins, carbohydrates, pigments and fatty acids. Although the production of microalgae has traditionally been photoautotrophic, these microorganisms have different forms of energy metabolism including heterotrophic and mixotrophic, which use an organic carbon source for the growth and production of biomass. The understanding of these metabolisms allows the diversification of current growth systems aiming at increasing the production of biomass and certain specific metabolites.
Photoautotrophic growth is the most common way to cultivate microalgae through photosynthesis. In these systems, high concentrations of CO2 are sequestered, but productivity is low when compared to heterotrophic and mixotrophic systems that provide high yields of biomass and secondary metabolites [51, 52]. Through photobioreactors is possible to obtain the maximum cell density of 40 g/L, while in outdoor open-pond or raceway-pond cultures, the cell concentration is usually lower than 10 g/L. This significantly increases the energy consumption of cell harvesting and the cost of biomass production [53] Usually scale-up of microalgae cultivation in wastewater is fulfilled phototrophically, which may be hindered by inefficient illumination and the low biomass density, leading to poor removal of nutrients [54].
For photosynthesis, light is used as an energy source and CO2 is used as a carbon source [55]. The carbon source is essential for growth and the higher its concentration, the higher the productivity. Nitrogen sources in the culture medium are also essential for the synthesis of proteins, nucleic acids and other biocomposites necessary for cell growth and survival [56] and the concentration must be compatible with the amount of carbon in the medium [6]. The type of cultivation, the nutrients, the carbon source, the salinity of the medium, the irradiance and the temperature vary according to the chosen species and also considerably influence the success of the microalgae production.
Microalgae can grow in the absence of light in culture media assimilating organic carbon. Studies show that some species, including Chlorella, C. protothecoides, C. vulgaris, C. zofingensis, C. minutissima, Tetraselmis and Neochloris [57] are able to grow in both autotrophic and heterotrophic conditions [56]. According to Hosoglu et al. [58], microalgae of the Chlorella Beyerinck genus are those that have the greatest potential for large-scale heterotrophic production, with emphasis on the species C. protothecoides that has been widely studied.
In heterotrophic crops, microalgae acquire carbon and energy from organic sources via oxidative phosphorylation, consuming O2 and releasing CO2. According to Behrens [59], the cost of producing the kg of dry biomass produced in photoautotrophic conditions can be 5.5 times higher than in heterotrophic conditions. In heterotrophic systems there are no light limitation problems, since microalgae grow in the absence of light using organic carbon as a carbon and energy source reaching high concentrations of biomass reaching up to 100 g/L, which considerably facilitates the harvesting process [60]. In heterotrophic processes, 18% of the energy obtained can be converted into adenosine triphosphate (ATP) whereas in photoautotrophic cultures this percentage is only 10% [61]. However, despite the advantages, the cultivation of microalgae under heterotrophic conditions, due to the use of organic carbon, requires reactors and techniques of greater complexity and high cost to avoid contamination caused by other microorganisms.
Under mixotrophic conditions, microalgae grow both photoautotrophically and heterotrophically, being able to assimilate organic compounds as a carbon source and use inorganic carbon as an electron donor [62]. In this metabolism, the energy is captured through the catalysis of external organic compounds through respiration and the light energy is converted into chemical compounds via photosynthesis, being a promising solution in the processes of environmental remediation, being able to treat the effluents of the agribusiness and produce biomass rich in metabolites of industrial interest.
In photoautotrophic crops, self-shade caused by the high density of cells makes light penetration difficult, causing photoinhibition and may be the limiting factor to its propagation leading to low biomass yields. Under heterotrophic conditions, not all microalgae species are able to grow and the strict use of only organic substrates as a source of carbon and energy makes the process more prone to contamination. Thus, an alternative to maximize production can be through mixotrophic cultivation. Therefore, the cells would multiply with autotrophic metabolism until reaching the maximum cell density, at which point a source of organic carbon is added to stimulate, also, heterotrophic growth. Thus, due to the high cell density in the medium, problems with contamination of microorganisms would be less likely to happen. For the success of this technique, the cultivated species must be able to grow in heterotrophic conditions without microbial contamination and the organic compound to be added, as well as its ideal concentration must be known.
Reducing use of light in mixotrophic processes decreases the demand for energy, which minimizes the operational cost in processes with artificial light. According to Perez-Garcia and Bashan [63] in these systems there is a better control capable of regulating the growth rate of the species, which minimizes the risk of contamination by photosynthetic microorganisms. Due to the significant heterotrophic contribution of the organic fraction, the reactor design does not require a maximized area to expose the microalgae to light to perform photosynthesis, decreasing the process cost.
According to Patel et al. [7], mixotrophic cultivation has advantages over photoautotrophic and heterotrophic metabolism. In this process, in addition to the higher growth rates reducing the microalgae growth cycle, there is also growth in the dark phase mediated by respiration, potentiating the production of biomass. There is also a comparatively prolonged exponential growth phase, great flexibility to change the metabolism from heterotrophic to photo-autotrophic and vice versa, prevention of photo-oxidative damage caused by O2 accumulated in closed photobioreactors and reduction in substrate uptake photoinhibition. It has been shown that microalgae cultivated under mixotrophic conditions can present, under controlled conditions, higher biomass productivity when compared to photoautotrophic and heterotrophic cultures [64].
The advancement of agro-industry has generated a large amount and variety of waste causing serious environmental problems and is one of the sectors that generate more waste rich in organic matter. According to Dahiya et al. [65], approximately 1.3 billion tons of foods are wasted each year during its production, handling, storage, processing, distribution or consumption. The composition of food processing residues is extremely varied and depends on both the nature of the raw material and the production technique employed.
Due to the scarcity of available areas close to large urban centers for the disposal of industrial and urban waste, the vast majority of companies do not carry out treatment and/or correct disposal of this material, which contributes to the increase in environmental pollution. Pollution is due to high concentrations of organic matter and heavy metals causing contamination, eutrophication of water bodies, death of aquatic organisms and local vegetation, ecological imbalance and health problems for the population. In this sense, the use of agro-industrial waste as a source of organic carbon for the cultivation of microalgae is presented as an option for the bioremediation of these effluents added to the production of biomass rich in biocompounds with different applications.
A lot of studies have evaluated the mixotrophic growth of microalgae using glucose, glycerol and acetate as a source of organic carbon and observed that the biomass yields were higher, which could decrease the cost of the process. Liang et al. [66] investigated C. vulgaris strain under autotrophic, mixotrophic and heterotrophic growth conditions. Mixotrophic growing on glucose with light produced the highest lipid productivity compared with other growth modes. Garcia et al. [67] studied the mixotrophic growth of tricornutum UTEX-640 using acetate, lactic acid, glycine, glucose and glycerol. The best results were obtained using with urea, which resulted in maximum biomass and eicosapentaenoic acid productivities significantly higher than those obtained for the photoautotrophic control, which suggest the possibility of using mixotrophy for the mass production of microalgae. Cheirsilp & Torpee [68] cultivated Chlorella sp., Chlorella sp., Nannochloropsis sp. and Cheatoceros sp. under mixotrophic condition using glucose as source of organic carbon. They observed that the biomass and lipid production of all tested strains in mixotrophic culture were notably enhanced in comparison with photoautotrophic and heterotrophic cultures.
Due to the success of the microalgae mixotrophic cultivation method, recent studies have been evaluating the possibility of using residues from the agro-industry as source of organic matter as a strategy to treat the effluent, produce biomass and reduce the cost of the process.
Hu et al. [69] evaluated the mixotrophic cultivation of Chlorella sp. UMN271 utilizing swine manure as nutrient supplement for evaluate the nutrient removal efficiencies by alga. The results showed that addition of 0.1% (v/v) acetic, propionic and butyric acids, respectively, could promote algal growth, enhance nutrient removal efficiencies and improve total lipids productivities. They concluded that Chlorella sp. grown on acidogenically-digested manure could be used as a feedstock for high-quality biodiesel production.
Li et al. [70] investigated the effects of autotrophic and mixotrophic growth on cell growth and lipid productivity of green microalgae Chodatella sp and Piggery wastewater served as nutrient sources for mixotrophic growth. The specific growth rate, biomass production, and lipid productivity obtained with mixotrophic growth were until 5.6 times higher than those obtained with autotrophic growth. The mixotrophic cultivation simultaneously assimilated 99.7% ammonia nitrogen and 75.9% total phosphorus from piggery wastewater, which reduced the required nutrient for the culture of microalgae, thereby reducing the cost of biomass for diverse application.
León-Vaz et al. [71] cultivated C. sorokiniana microalgae under mixotrophic conditions utilized Oxidized wine waste lees among other agro-industrial wastes as carbon source. The fed-batch strategy and the medium optimization, with nutrient supplementation, have been found to be very effective in enhancing biomass and neutral lipid productivity, suggesting that this is a promising strategy for production of microalgal biomass. The algal biomass concentration was 11 g L-1 with a lipid content of 38% (w/w).
Bhatnagar et al. [72] evaluated mixotrophic growth of Chlamydomonas globosa, Chlorella minutissima and Scenedesmus bijuga under medium supplemented with different organic carbon substrates and wastewaters. The mixotrophic growth of these microalgae resulted in 3–10 times more biomass production relative to phototrophy. Poultry litter extract as growth medium recorded up to 180% more biomass growth compared to standard growth medium, while treated and untreated carpet industry wastewaters also supported higher biomass, with no significant effect of additional nitrogen supplementation.
Andrade & Coosta [73] determined the effects of molasses concentration and light levels on mixotrophic biomass production by Spirulina platensis. Molasses concentration was the main factor influencing maximum biomass concentration (Xmax) reached 2.94 g L− 1 and μmax 0.147 d − 1. Molasses, suggesting that this industrial by-product could be used as a low-cost supplement for the growth of Spirulina platensis, stimulated the production of biomass.
Melo et al. [74] evaluated the growth, nutrients and toxicity removal of Chlorella vulgaris cultivated under autotrophic and mixotrophic conditions using corn steep liquor, cheese whey and vinasse as source of organic matter. The results demonstrated that corn steep liquor toxicity was totally eliminated and cheese whey and vinasse toxicity were minimized by C. vulgaris. They demonstrated that the mixotrophic cultivation of C. vulgaris is able to increase cellular productivity and could be an alternative to remove the toxicity from agroindustrial by-products.
Hugo et al. [75] studied the growth of forty microalgae strains under mixotrophic conditions using sugarcane vinasse as source of organic matter. Micractinium sp. Embrapa|LBA32 and C. biconvexa Embrapa|LBA40 presented expressive growth in a light-dependent manner even in undiluted vinasse under non-axenic conditions. Microalgae strains presented higher biomass productivity in vinasse-based medium compared to autotrophic medium. This research showed the potential of using residues derived from ethanol plants to cultivate microalgae for the production of energy and bioproducts.
Mitra et al. [76] cultivated Chlorella vulgaris under mixotrophic/heterotrophic conditions using dry-grind ethanol thin stillage and soy whey as nutrient feedstock. The results showed the biomass yields from thin stillage, soy whey and modified basal medium after 4 days of incubation at mixotrophic conditions in the bioreactor were 9.8, 6.3 and 8.0 g.L− 1 with oil content at 43, 11, and 27% (w/w) respectively. This research highlights the potential of these agro-industrial co-products as microalgal growth media with consequent production of high-value microalgal oil and biomass.
Salati et al. [77] cultivated Chlorella vulgaris using cheese whey, white wine lees and glycerol as carbon sources under mixotrophic conditions. The mixotrophic biomass production was1.5–2 times higher than autotrophic growth. Furthermore, it gave much higher energy recovery efficiency, i.e. organic carbon energy efficiency of 32% and total energy efficiency of 8%, suggesting the potential for the culture of algae as a sustainable practice to recover efficiently waste-C and produce biomass.
Piasecka et al. [78] studied the growth of Tetradesmus obliquus by supplementation with beet molasses in photoheterotrophic and mixotrophic culture conditions. The highest protein content was obtained in the mixotrophic growth suggesting this metabolism promising for protein production.
Tsolcha et al. [79] evaluated a mixed cyanobacterial-mixotrophic algal population, dominated by the filamentous cyanobacterium Leptolyngbya sp. and the microalga Ochromonas under non-aseptic conditions for its efficiency to remove organic and inorganic compounds from second cheese whey, poplar sawdust, and grass hydrolysates. Nutrient removal rates, biomass productivity, and the maximum oil production rates were determined. The highest lipid production was achieved using the biologically treated dairy effluent (up to 14.8% oil in dry biomass corresponding to 124 mg L − 1), which also led to high nutrient removal rates (up to 94%). Lipids synthesized by the microbial consortium contained high percentages of saturated and mono-unsaturated fatty acids (up to 75% in total lipids) for all the substrates tested, which implies that the produced biomass may be harnessed as a source of biodiesel.
Grupta et al. [80] cultivated the Chlorella microalgae under mixotrophic conditions using a raw food-processing industrial wastewater. About 90% reduction in TOC and COD were obtained for all dilutions of wastewater. Over 60% of nitrate and 40% of phosphate were consumed by microalgae from concentrated raw wastewater. The degradation kinetics also suggested that the microalgae cultivation on a high COD wastewater is feasible and scalable.
Yeesang et al. [81] evaluated B. braunii, a microalgae rich in oil under mixotrophic cultivation using molasses, a cheap by-product from the sugar cane plant as a carbon source and under photoautotrophic cultivation using nitrate-rich wastewater supplemented with CO2. The mixotrophic cultivation produced a high amount of biomass of 3.05 g L − 1 with a high lipid content of 36.9%. The photoautotrophic cultivation in nitrate-rich wastewater supplemented with 2.0% CO2 produced a biomass of 2.26 g L − 1 and a lipid content of 30.3%. They showed that these strategies could be promising ways for producing cheap lipid-rich microalgal biomass as biofuel feedstock and animal feeds.
Gélinas et al. [82] studied the mixotrophic growth and lipid production of Chlorella consortium using residual corn hydrolysate and corn silage juice as source of organic and compared to heterotrophic conditions. Maximum microalgal biomass of 0.8 g/L was obtained with 1 g/L of residual corn hydrolysate whatever the trophic strategy. Under mixotrophic conditions, the use of residual corn hydrolysate led to an increase of 21% and 22% in comparison with the biomass produced with glucose or silage juice, respectively. This increase varied between 11% and 28% under heterotrophic condition. They observed that at the end of the experiment, algae exposed to silage juice decreased significantly. Residual corn hydrolysate represented an interesting and efficient alternative as an organic carbon source. However, silage juice needs additional treatments to be implemented as a culture medium.
Nur et al. [83] studied palm oil mill effluent (POME), one of the wastewaters generated from palm oil mills, as source of organic carbon for mixotrophic microalgae growth. The aim of this research was to identify the growth of Chlorella vulgaris cultured in POME medium under mixotrophic conditions in relation to a variety of organic carbon sources added to the POME mixture. The research was conducted with 3 different carbon sources (D-glucose, crude glycerol and NaHCO3) in 40% POME. They showed that C. vulgaris using D-glucose as carbon source gained a lipid productivity of 195 mg/l/d.
Manzoor et al. 2020 presented the growth of Scenedesmus dimorphus NT8c cultivated mixotrophically on sugarcane bagasse hydrolysate, a low-value agricultural by-product. Under mixotrophic conditions the S. dimorphus NT8c showed higher growth rates compared to photoautotrophic cultivation and the biomass productivity was 119.5 mg L d − 1, protein contents was 34.82% and fatty acid contents was 15.41%. They concluded that mixotrophically-cultivated microalgae are able to increase the biomass and lipid productivity. However, the concentrations of supplementation need to be studied because higher level of organic carbon can result in unfavorable levels of turbidity and bacterial growth, reducing microalgal biomass productivity.
Microalgal biomass represents a sustainable alternative to fossil consumption and bioproducts for food and pharmaceutical industry. Microalgae can growth under photoautotrophic, heterotrophic or mixotrophic modes where the latter two trophic modes require organic carbon to grow efficiently. Actually, researchers have highlighted the role of low cost-efficient agro-industrial by-products used as supplements in algal culture media. However, supplementation of organic carbon contributes significantly to a higher cost of microalgae production and this can compete with human and animal alimentation. Agro-industrial by-products and wastes are of great interest as cultivation medium for microorganisms because of their low cost, renewable nature, and abundance.
Faced with this scenario, biotechnological technologies are necessary to develop the production of microalgae on a large scale and expand the range of utilities that, in the short or long term, contribute to the improvement of industrial processes. In addition, mixotrophic microalgae growth is a great strategy to reduce environmental pollution generated by residues rich in organic matter and can reduce the cost of the industrial process. However, more investments, development and greater knowledge of the metabolism of these microalgae and their effectiveness in the generation of new bioproducts are increasingly necessary.
The authors gratefully acknowledge the Postgraduation Dean’s Office of the Federal University of Rio Grande do Norte and Dean of Extension of Federal Institute of Rio Grande do Norte. The authors would like to thank Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for the financial support.
As a company committed to the wider dissemination of knowledge, IntechOpen supports the OAI Metadata Harvesting Protocol (OAI-PMH Version 2.0).
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\\n\\nWe have adopted the Protocol to increase the number of readers of our publications. All our Works are more widely accessible, with resulting benefits for scholars, researchers, students, libraries, universities and other academic institutions. Through this method of exposing metadata, IntechOpen enables citation indexes, scientific search engines, scholarly databases, and scientific literature collections to gather metadata from our repository and make our publications available to a broader academic audience.
\\n\\nAs a Data Provider, metadata for published Chapters and Journal Articles are available via our interface at the base URL:http://www.intechopen.com/oai/?.
\\n\\nREQUESTS
\\n\\nYou can find out more about the Protocol by visiting the Open Archives website. For additional questions please contact us at info@intechopen.com.
\\n\\nDATABASES
\\n\\nDatabases, repositories and search engines that provide services based on metadata harvested using the OAI metadata harvesting protocol include:
\\n\\nBASE - Bielefeld Academic Search Engine
\\n\\nOne of the world's most powerful search engines, used primarily for academic Open Access web resources.
\\n\\n\\n\\nA search engine for online catalogues of publications from all over the world.
\\n"}]'},components:[{type:"htmlEditorComponent",content:'The OAI-PMH (Open Archives Initiative Protocol for Metadata Harvesting) is used to govern the collection of metadata descriptions and enables other archives to access our database. The Protocol has been developed by the Open Archives Initiative, based on ensuring interoperability standards in order to ease and promote broader and more efficient dissemination of information within the scientific community.
\n\nWe have adopted the Protocol to increase the number of readers of our publications. All our Works are more widely accessible, with resulting benefits for scholars, researchers, students, libraries, universities and other academic institutions. Through this method of exposing metadata, IntechOpen enables citation indexes, scientific search engines, scholarly databases, and scientific literature collections to gather metadata from our repository and make our publications available to a broader academic audience.
\n\nAs a Data Provider, metadata for published Chapters and Journal Articles are available via our interface at the base URL:http://www.intechopen.com/oai/?.
\n\nREQUESTS
\n\nYou can find out more about the Protocol by visiting the Open Archives website. For additional questions please contact us at info@intechopen.com.
\n\nDATABASES
\n\nDatabases, repositories and search engines that provide services based on metadata harvested using the OAI metadata harvesting protocol include:
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\n\nOne of the world's most powerful search engines, used primarily for academic Open Access web resources.
\n\n\n\nA search engine for online catalogues of publications from all over the world.
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